Odour intensity learning in fruit flies

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1672, 2009, Pages 3413-3420

  Yarali, Ayse ^a,d   Ehser, Sabrina ^a   Hapil, Fatma Zehra ^a,b   Huang, Ju ^a,c   Gerber, Bertram ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b BILKENT UNIVERSITY   (Turkey)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Associative learning; Benzaldehyde; Fruit fly; Odour intensity; Olfaction; Recognition

Indexed keywords

BENZALDEHYDE;

FLY; LEARNING; MOLECULAR ANALYSIS; NEUROLOGY; ODOR; OLFACTION; RECOGNITION;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN FUNCTION; DROSOPHILA MELANOGASTER; ELECTRIC SHOCK; MEMORY; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; TRAINING;

ANIMALIA; DROSOPHILA MELANOGASTER;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); DROSOPHILA MELANOGASTER; LEARNING; ODORS;

EID: 70349610078     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.0705     Document Type: Article

References (50)

1. Acevedo, S. F., Froudarakis, E. I., Tsiorva, A. A. & Skoulakis, E. M. 2007 Distinct neuronal circuits mediate experience-dependent, non-associative osmotactic responses in Drosophila. Mol. Cell. Neurosci. 34, 378-389. (doi:10.1016/j.mcn.2006.11.011)
2. Ache, B. W. & Young, J. M. 2005 Olfaction: diverse species, conserved principles. Neuron 48, 417-430. (doi:10.1016/ j.neuron.2005.10.022)
3. Ayer, R. K. & Carlson, J. 1992 Olfactory physiology in the Drosophila antenna and maxillary palp: acj6 distinguishes two classes of odorant pathways. J. Neurobiol. 23, 965-982. (doi:10.1002/neu.480230804)
4. Bargmann, C. I. 2006 Comparative chemosensation from receptors to ecology. Nature 444, 295-301. (doi:10.1038/nature05402)
5. Benton, R. 2006 On the ORigin of smell: odorant receptors in insects. Cell. Mol. Life Sci. 63, 1579-1585. (doi:10.1007/s00018-006-6130-7)
6. Borst, A. 1981 Computation of olfactory signals in Drosophila melanogaster. J. Comp. Physiol. A 152, 373-383. (doi:10.1007/BF00606242)
7. Boyle, J. & Cobb, M. 2005 Olfactory coding in Drosophila larvae investigated by cross-adaptation. J. Exp. Biol. 208, 3483-3491. (doi:10.1242/jeb.01810)
8. Brand, A. H. & Perrimon, N. 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415. (Pubitemid 23214028)
9. Buck, L. B. 1996 Information coding in the vertebrate olfactory system. Annu. Rev. Neurosci. 19, 517-544. (doi:10.1146/annurev.ne.19.030196.002505)
10. Colomb, J., Grillenzoni, N., Stocker, R. F. & Ramaekers, A. 2007 Complex behavioural changes after odour exposure in Drosophila larvae. Anim. Behav. 73, 587-594. (doi:10. 1016/j.anbehav.2006.04.016)
11. Dahanukar, A., Hallem, E. A. & Carlson, J. R. 2005 Insect chemoreception. Curr. Opin. Neurobiol. 15, 423-430. (doi:10.1016/j.conb.2005.06. 001)
12. DasGupta, S. & Waddell, S. 2008 Learned odor discrimination in Drosophila without combinatorial odor maps in the antennal lobe. Curr. Biol. 18, 1668-1674. (doi:10. 1016/j.cub.2008.08.071)
13. Davis, R. L. 2004 Olfactory learning. Neuron 44, 31-48. (doi:10.1016/j.neuron.2004.09.008)
14. Duffy, J. B. 2002 GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34, 1-15. (doi:10.1002/gene. 10150)
15. Fiala, A. 2007 Olfaction and olfactory learning in Drosophila: recent progress. Curr. Opin. Neurobiol. 17, 720-726. (doi:10.1016/j.conb.2007.11.009)
16. Galizia, C. G. & Menzel, R. 2000 Odor perception in honeybees: coding information in glomerular patterns. Curr. Opin. Neurobiol. 10, 504-510. (doi:10.1016/ S0959-4388(00)00109-4)
17. Gerber, B., Tanimoto, H. & Heisenberg, M. 2004 An engram found? Evaluating the evidence from fruit flies. Curr. Opin. Neurobiol. 14, 737-744. (doi:10.1016/j. conb.2004.10.014)
18. Gerber, B., Stocker, R. F., Tanimura, T. & Thum, A. S. 2009 Smelling, tasting, learning: Drosophila as a study case. Results Probl. Cell Differ. 47, 139-185.
19. Godenschwege, T. A. et al. 2004 Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur. J. Neurosci. 20, 611-622. (doi:10.1111/ j.1460-9568.2004.03527.x)
20. Hallem, E. A., Dahanukar, A. & Carlson, J. R. 2006 Insect odor and taste receptors. Annu. Rev. Entomol. 51, 113-135. (doi:10.1146/annurev.ento.51. 051705.113646)
21. Helfand, S. L. & Carlson, J. R. 1989 Isolation and characterization of an olfactory mutant in Drosophila with a chemically specific defect. Proc. Natl Acad. Sci. USA 86, 2908-2912. (doi:10.1073/pnas.86.8.2908)
22. Hildebrand, J. C. & Shepherd, G. M. 1997 Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595-631. (doi:10.1146/annurev.neuro.20.1.595)
23. Johnson, B. A. & Leon, M. 2007 Chemotopic odorant coding in a mammalian olfactory system. J. Comp. Neurol. 503, 1-34. (doi:10.1002/cne.21396)
24. Keene, A. C., Stratmann, M., Keller, A., Perrat, P. N., Vosshall, L. B. &Waddell, S. 2004 Diverse odor-conditioned memories require uniquely timed dorsal paired medial neuron output. Neuron 44, 521-533. (doi:10.1016/j. neuron.2004.10.006)
25. Korsching, S. 2002 Olfactory maps and odor images. Curr. Opin. Neurobiol. 12, 387-392. (doi:10.1016/S0959-4388(02)00348-3)
26. Laberge, F. & Hara, T. J. 2001 Neurobiology of fish olfaction: a review. Brain Res. Rev. 36, 46-59. (doi:10.1016/S0165-0173(01)00064-9)
27. Lai, S. L., Awasaki, T., Ito, K. & Lee, T. 2008 Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 135, 2883-2893. (doi:10.1242/dev.024380)
28. Laurent, G., Stopfer, M., Friedrich, R. W., Rabinovich, M. I., Volkovskii, A. & Abarbanel, H. D. 2001 Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu. Rev. Neurosci. 24, 263-297. (doi:10.1146/annurev.neuro.24.1.263)
29. Mainen, Z. F. 2006 Behavioral analysis of olfactory coding and computation in rodents. Curr. Opin. Neurobiol. 16, 429-434. (doi:10.1016/j.conb. 2006.06.003)
30. Masek, P. & Heisenberg, M. 2008 Distinct memories of odour intensity and quality in Drosophila. Proc. Natl Acad. Sci. USA 105, 15 985-15 990. (doi:10.1073/pnas. 0804086105)
31. Michels, B., Diegelmann, S., Tanimoto, H., Schwenkert, I., Buchner, E. & Gerber, B. 2005 A role for Synapsin in associative learning: the Drosophila larva as a study case. Learn. Mem. 12, 224-231. (doi:10.1101/lm. 92805)
32. Ng, M., Roorda, R. D., Lima, S. Q., Zemelman, B. V., Morcillo, P. & Miesenböck, G. 2002 Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474. (doi:10.1016/S0896-6273(02)00975-3) (Pubitemid 35284733)
33. Pan, Y., Zhou, Y., Guo, C., Gong, H., Gong, Z. & Liu, L. 2009 Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory. Learn. Mem. 16, 289-295. (doi:10.1101/lm.1331809)
34. Pelz, C., Gerber, B. & Menzel, R. 1997 Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation. J. Exp. Biol. 200, 837-847.
35. Phelps, C. B. & Brand, A. H. 1998 Ectopic gene expression in Drosophila using GAL4 system. Methods 14, 367-379. (doi:10.1006/meth.1998.0592)
36. Preat, T. 1998 Decreased odor avoidance after electric shock in Drosophila mutants biases learning and memory tests. J. Neurosci. 18, 8534-8538. (Pubitemid 28465027)
37. Sachse, S. & Galizia, G. 2003 The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur. J. Neurosci. 18, 2119-2132. (doi:10.1046/j.1460-9568.2003.02931.x)
38. Schwaerzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S. & Heisenberg, M. 2003 Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23, 10 495-10 502. (Pubitemid 37485262)
39. Shang, Y., Claridge-Chang, A., Sjulson, L., Pypaert, M. & Miesenböck, G. 2007 Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128, 601-612. (doi:10.1016/j.cell.2006.12.034) (Pubitemid 46198891)
40. Strausfeld, N. J. & Hildebrand, J. G. 1999 Olfactory systems: common design, uncommon origins? Curr. Opin. Neurobiol. 9, 634-639. (doi:10.1016/S0959-4388(99)00019-7)
41. Tully, T. & Quinn, W. G. 1985 Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A 157, 263-277. (doi:10.1007/ BF01350033)
42. Turner, G., Bazhenov, M. & Laurent, G. 2008 Olfactory representations by mushroom body neurons. J. Neurophysiol. 99, 734-746. (doi:10.1152/jn.01283. 2007) (Pubitemid 351253231)
43. Voeller, T. 2009 Visualisierung und Manipulation neuronaler Aktivitäten im Gehirn von Drosophila melanogaster. PhD thesis, Universität Würzburg, Würzburg, Germany.
44. Vosshall, L. B. 2000 Olfaction in Drosophila. Curr. Opin. Neurobiol. 10, 498-503. (doi:10.1016/S0959-4388(00) 00111-2)
45. Vosshall, L. B. & Stocker, R. F. 2007 Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30, 505-533. (doi:10.1146/ annurev.neuro.30.051606.094306)
46. 2+ imaging. J. Neurosci. 24, 6507-6514. (doi:10.1523/ JNEUROSCI.3727-03.2004)
47. Wilson, R. & Laurent, G. 2005 Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069-9079. (doi:10.1523/JNEUROSCI.2070-05.2005) (Pubitemid 41500816)
48. Wright, G. A., Thomson, M. G. & Smith, B. H. 2005 Odour concentration affects odour identity in honeybees. Proc. Biol. Sci. 272, 2417-2422. (doi:10.1098/rspb.2005.3252)
49. Xia, S. & Tully, T. 2007 Segregation of odor identity and intensity during odor discrimination in Drosophila mushroom body. PLOS Biol. 5, 2398-2407. (doi:10. 1371/journal.pbio.0050264) (Pubitemid 350035437)
50. Yarali, A., Mayerle, M., Nawroth, C. & Gerber, B. 2008 No evidence for visual context-dependency of olfactory learning in Drosophila. Naturwissenschaften 95, 767-774. (doi:10.1007/s00114-008-0380-1)